Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:
Tree Physiology 16, 109--114
© 1996 Heron Publishing----Victoria, Canada
Shade-shoot structure, photosynthetic performance in the field, and
photosynthetic capacity of evergreen conifers
JERRY W. LEVERENZ
Department of Ecology and Environmental Sciences, Swedish University of Agricultural Sciences, Box072,
7 S-750 07 Uppsala, Sweden
Current address: The Arboretum, The Royal Veterinary and Agricultural University, Kirkegaardsvej 3A,
DK2970 Hoersholm, Denmark
Received March 2, 1995
Summary Shoot structure can be quantified as the ratio of
maximum shoot silhouette area to maximum leaf silhouette
(projected) area (Rmax ). I have used published studies on the
effects of shade-shoot structure on photosynthetic production
of evergreen conifer stands to test the hypothesis that the lower
crown of stands of species with a high Rmax contributes significantly to photosynthetic production. Pruning studies were
found inadequate to test this hypothesis rigorously. Eight studies that used cuvettes to measure photosynthetic production in
different crown layers are reviewed. Of six studies on species
with Rmax values larger than 0.7, five found significant rates of
photosynthesis in the lower half of the crowns. In contrast,
pines, which have a low Rmax and a low leaf area index (≤ 3.5),
had low rates of photosynthesis in the lowest crown zone. In
field-grown shoots of all species examined, photosynthetic
capacity was negatively related to Rmax .
Keywords: field photosynthesis, leaf silhouette area, photosynthetic production, shoot silhouette area.
Introduction
Leverenz and Hinckley (1990) and Leverenz (1992) found
significant correlations between the architecture of shade
shoots (quantified as the ratio of maximum shoot silhouette
area to maximum leaf silhouette (projected) area, Rmax ) of
different evergreen conifer species and maximum leaf area
index, or maximum stand production. These correlations support the hypothesis that, in closed evergreen conifer stands, the
distribution and inclination of needles within shade-adapted
shoots has a major effect on maximum photosynthetic production and thus maximum stand production. However, this positive correlation does not hold on all sites, and species that are
more productive on good sites can be less productive on poor
sites (Aldhous and Low 1974). Thus shoot architecture can
affect the ability of a species to respond to variations in nutrient
availability or site water balance.
Leverenz and Hinckley (1990) hypothesized that species
that produce shade shoots with a high Rmax will be able to
develop a deeper canopy in terms of leaf area or leaf biomass
as a result of a lower light compensation point than shade
shoots with a low Rmax . It was also hypothesized that shade
shoots with a high Rmax will operate more efficiently at irradiances just above the light compensation point than shade
shoots with a low Rmax . This would result in significant photosynthetic production even at irradiances only slightly above
the light compensation point. I have reviewed the literature on
photosynthetic production at different canopy depths within
stand-grown trees to determine whether species that have a
high Rmax also have a high leaf area index and significant
photosynthetic production in their lower crowns. Conversely, I
have also examined whether species with a low Rmax have a low
leaf area index and negligible photosynthetic production in
their lower crowns.
Leverenz (1995) reported laboratory data indicating that
shade-shoot structure itself is responsible for the correlations
between Rmax and stand production through its effect on photosynthetic efficiency. In the same study, no clear effects of
variation in needle structure were observed. However, the
illumination used was strongly collimated or almost totally
diffuse, which is not the case in nature (Madgwick and Brumfield 1969, Grace 1971). Also, these laboratory measurements
were made under steady-state conditions, and it is not known
how natural fluctuations in irradiance with time may affect the
results. For example, under natural illumination, a pine shoot
may be no less photosynthetically efficient than a flat shoot
because the changing position of the sun results in shadows
that constantly move across individual cells of the needles, i.e.,
spatial and temporal variations in illumination direction may
compensate for differences in shoot structure so that, if the
pattern of shadows occurs with the right frequency, decreases
in photosynthesis as a result of mutual shading may be small
(Pearcy 1990). A second objective of this review, therefore,
was to survey the literature to test the hypothesis that photosynthetic performance in the field is related to shoot architecture.
Pruning experiments
Pruning or thinning experiments often result in the conclusion
that the lower crown of conifer canopies does not contribute
significantly to the production of the stand. For example,
Waring (1991) concluded that leaf area indices in excess of 6
are inconsequential for photosynthetic production. However,
110
LEVERENZ
based on a review of pruning experiments within forest stands,
Mar-Møller (1960) concluded the lower crown zones are important for photosynthetic production. He found that in cases
where pruning the lower branches from forest trees did not
decrease production, other factors were confounding the results. Thus in some studies, the foliage removed by pruning
was largely or completely replaced by regrowth, and so no
statistically significant effects of pruning were found. In other
studies, there was no measurable effect of pruning on stem
growth because pruning was done below the height on the stem
where diameter growth was measured (Margolis et al. 1988).
Mar-Møller (1960) also reported a study (Hartig 1872)
where severe drought in combination with pruning resulted in
an increase in production. It is probable that there is an optimal
leaf area index that is a function of site water balance (Gholz
et al. 1976, Linder 1985). Pruning of stands with a supra-optimal leaf area index as a result of drought stress should lead to
a less negative, or even a positive effect on growth. This would
occur when leaf water potentials drop below a critical water
potential for growth (Hsiao 1973) or photosynthesis (Aussenac
and Granier 1978, Beadle et al. 1981). Therefore, to interpret
accurately the results of pruning experiments, the effects of
limiting water on tree growth must be clearly separated from
the contribution of the lower canopy to photosynthetic production. There is good evidence that leaf area in evergreen conifers
is controlled by Rmax through its affect on the light compensation point (Leverenz and Hinckley 1990, Leverenz 1995).
Thus, it may be hypothesized that there is selection pressure
for a particular Rmax (low Rmax on drought-prone sites and high
Rmax on well-watered sites) to obtain an optimal leaf area for
maximizing tree growth and reproductive success.
Pruning of the lower crown zone may have little effect on
growth in some instances simply because only a small fraction
of the total leaf area or mass is removed. Oren et al. (1986)
found that, in Picea abies (L.) Karst., the lower 40% of the
canopy in terms of height contains only 5% of the foliage mass.
Similarly, in Pseudotsuga menziesii (Mirb.) Franco, the lower
25 to 30% of the canopy (based on whorl number) may contain
only 4 to 9% of the foliage mass (Jensen 1976, Brix 1981).
I conclude that most published pruning studies do not provide a critical test of the hypothesis that the lowest one-third
of the leaf mass or leaf area of a canopy contributes significantly to total canopy photosynthetic production.
Photosynthetic production within different crown zones
I found eight published studies on four species of evergreen
conifers that reported on variation in photosynthetic production with crown depth. The species studied were: P. menziesii
(Woodman 1971, Künstle and Mitscherlich 1975), P. abies
(Neuwirth 1968, Oren et al. 1986, Häsler 1992), Picea sitchensis (Bong.) Carr. (Watts et al. 1976), and Pinus sylvestris L.
(Neuwirth 1972, Künstle and Mitscherlich 1975, Beadle et al.
1985). Table 1 lists the results from this survey in order of
decreasing Rmax and decreasing maximum leaf area index.
Assuming the stands were not subject to severe stress, the LAI
was substantially more than 6 for all species except
Table 1. Relative photosynthetic production within different crown
zones of stand-grown trees.
Species
Percent of maximum photosynthesis
Dry weight basis
Area basis
Pseudotsuga menziesii (Woodman 1971)
Rmax = 0.87, LAImax = 13
Level 1 (top)
84%
Level 2
100%
Level 3
71%
Level 4 (bottom)
11%
Picea abies (Neuwirth 1968; combined results from extreme types
of comb and plate spruces)
Rmax = 0.84, LAImax = 11.5
Level 1 (top)
100%
Level 2
80%
Level 3
64%
Level 4 (bottom)
> 26%
Picea abies (Oren et al. 1986)
Rmax = 0.84, LAImax = 11.5
Level 1 (top)
Level 2
Level 3
Level 4 (bottom)
100%
97%
70%
52%
93%
100%
57%
33%
Picea sitchensis (Watts et al. 1976)
Rmax = 0.74, LAImax = 10.6
Level 1 (Nodes 1--3, top)
100%
Level 2 (Nodes 4--6)
99%
Level 3 (Nodes 7--8, bottom)
62%
100%
79%
42%
Pinus sylvestris (Neuwirth 1972)
Rmax = 0.54, LAImax = 3.5
Level 1 (12--15 m)
100%
Level 2 (9--12 m)
70%
Level 3 (6--9 m)
28%
Pinus sylvestris (Beadle et al. 1985)
Rmax = 0.54, LAImax = 3.5
Level 1(top)
Level 2 (middle)
Level 3 (bottom)
100%
66%
34%
P. sylvestris. The data of Häsler (1992) and Künstle and Mitscherlich (1975) are not listed in Table 1 because they sampled
at only two heights in the tree crowns and used a limited
number of cuvettes.
Based on the data reported by Woodman (1971) for
P. menziesii (Rmax = 0.87), photosynthetic production was only
negligible in the lowest crown zone (Level 4). This zone
contained 10% of the living branches of the tree, but less than
10% of the total foliage mass, and represented the zone where
shoots die for lack of light. The bulk of the crown (90%) had
rates of photosynthesis that were 70% of the zone with the
highest rates.
Similar results were obtained for P. abies (Rmax = 0.84)
based on the data in Figures 2 and 4 of the papers by Neuwirth
(1968) and Oren et al. (1986), respectively. In agreement with
Mar-Møller (1960), Neuwirth (1968) concluded that care
FIELD PHOTOSYNTHESIS AND SHADE-SHOOT STRUCTURE
should be taken not to underestimate the contribution of the
lower crown zone to the total photosynthetic production of the
entire crown. The study by Oren et al. (1986) showed that the
upper shade crown made a large contribution to photosynthetic
production per unit leaf area, especially when expressed per
unit of invested leaf mass (values obtained by dividing the
mean rates of photosynthesis by their mean specific leaf areas).
However, even in the lowest canopy zone, photosynthetic
production (dry weight basis) was 52% of that in the most
productive zone. Similarly, Häsler (1992) found that photosynthetic production (needle area basis) in the lower crown of a P.
abies tree was 56% of that in the upper crown. However, the
data reported by Häsler (1992) do not provide a rigorous test
of the hypothesis because it is unclear if the sampled trees were
growing in a closed stand.
A summary of data published by Watts et al. (1976) for
P. sitchensis is shown in Table 1. Rates of photosynthesis on an
area basis were calculated from their Figure 7, and data for the
same stand (Figure 7 in Norman and Jarvis 1974) were then
used to convert from an area to a mass basis. The relatively
high Rmax of 0.74 of P. sitchensis was associated with an LAI
substantially above 6 and with significant rates of photosynthesis (dry weight basis) in the lowest third of the crown (whorl
basis).
In contrast to the above five studies on species with shade
shoots with a high Rmax , Künstle and Mitscherlich (1975)
concluded that, in P. menziesii (Rmax = 0.87), the lower half of
the crown did not contribute significantly to photosynthetic
production. The reason for this discrepancy is unclear.
A comparison of the data for P. sitchensis, P. abies and
P. menziesii with the data for P. sylvestris (Rmax = 0.54) reported by Neuwirth (1972) and Beadle et al. (1985) indicated
that the lower crown zone of P. sylvestris was less productive
than the lower crowns of the other three species despite the
much lower LAI of the pine species. Both studies report that
photosynthetic production of the lowest crown zone was about
30% of that of the highest crown zone (Neuwirth 1972, Beadle
et al. 1985). Thus, the P. sylvestris canopies had both lower
LAI and lower rates of photosynthesis in their lower crown
compared with the upper crown. Unfortunately, it is not possible to relate these photosynthetic data for P. sylvestris to the
actual leaf area or leaf mass within the different canopy zones;
however, the maximum leaf area index for P. sylvestris is so
low (about 3, and at most 4) that the LAI of the total crown
would be equivalent to, or less than, the upper half of the
crowns of the other species. Nevertheless, there was still a
sharp decrease in photosynthetic performance with decreasing
crown depth in the P. sylvestris stands.
I conclude that five of these six studies support the hypothesis (Leverenz and Hinckley 1990) that species that produce
shade shoots with a high Rmax will have substantial rates of
photosynthesis in the bulk of their lower crowns despite having
an LAI of more than 6. Only the very lowest foliage (10% or
less of the total leaf mass) appears not to contribute significantly to total photosynthetic production.
111
Photosynthetic responses to light by individual shoots
To test the hypothesis that shoot architecture itself underlies
the observed differences in photosynthetic production. It is
necessary to test the effects under natural illumination. I compared the photosynthetic performance of different species
based on the following criteria: the initial slope of the irradiance response curve of photosynthesis (the maximum quantum
yield based on incident light), rate of dark respiration, light
compensation point, rate of bending of the light response curve
(apparent convexity), and maximum rate of photosynthesis
(Leverenz 1995).
Under nonstress conditions, the initial slope of the irradiance response curve of photosynthesis may be modeled as
(Leverenz 1995):
φi ≤ αφaRmax ,
(1)
where φi is the maximum initial slope (equivalent to apparent
quantum yield) based on incident irradiance, φa is the maximum initial slope based on absorbed irradiance or illuminance,
and α is leaf absorptance under the conditions of illumination.
Interceptance of irradiance will be reduced for all directions of
illumination other than the one that maximizes Rmax . This will
decrease the initial slope based on incident light. In the field,
φi will not be larger than φaRmax if the total irradiance at the
shoot is accurately estimated.
Troeng and Linder (1982) estimated that the mean maximum φi for P. sylvestris shoots in the field was 0.27 ± 0.002,
which when divided by 0.5 to correct for Rmax gives an estimated φa of 0.054. The expected quantum yield at 20 °C is
0.061 (Leverenz and Öquist 1987), which is about 12% higher
than predicted by Equation 1. On a projected needle area basis,
a φi of 0.052 is obtained from Figure 4 of the paper published
by Benecke (1980), which when divided by 0.5 to correct for
Rmax gives a φa of 0.104 compared with an expected yield at
17 °C of 0.063 (Leverenz and Öquist 1987). In this case, the
apparent quantum yield is 1.65 times higher than predicted by
Equation 1. Dick et al. (1991) also reported high φi values for
Pinus contorta Dougl. shoots.
One of the few comparisons of light response curves of
photosynthesis of different conifer species under natural illumination was made by Künstle and Mitscherlich (1970), who
compared the light response curves of shoots of P. menziesii
and P. sylvestris. The P. menziesii shoot probably did not
receive direct solar radiation until after 1500 h, whereas the
P. sylvestris shoot did not receive direct solar radiation in the
afternoon. Parameter values describing the curves were obtained by nonlinear least squares fitting of the convexity equation to these data (Figure 1). The estimated φi of the fitted curve
for P. sylvestris was 0.53 times the φi value for P. menziesii.
From a regression equation relating shoot architecture to φi
determined in the laboratory, Leverenz (1995) predicted a ratio
of 0.61 assuming Rmax values of 0.87 and 0.5 for the P. menziesii and P. sylvestris shoots, respectively. However, when the
field and laboratory φi values were corrected for possible
differences in specific leaf area between the two species:
112
LEVERENZ
Figure 1. Net photosynthesis (An ) in relation to illuminance for a
Pseudotsuga menziesii shoot (s) and a Pinus sylvestris shoot (d).
Illuminance was measured with a spherical sensor. Data points were
taken from Figure 5 in Künstle and Mitscherlich (1970). The solid
lines represent the best fit of the convexity equation to the data by
nonlinear least squares.
φi,weight ≤ αφaRmax /S,
(2)
where S is the specific leaf area in units of m2 g −1, the φi,weight
values determined from field measurements were not significantly different from those predicted from laboratory measurements.
The rates of dark respiration estimated by fitting the convexity equation were similar for the two species (0.12 mg g −1 h −1)
(cf. Hodges and Scott 1968, Leverenz 1995). The light compensation point (Γi) was twofold higher for P. sylvestris (1.2
Klux) than for P. menziesii (0.6 Klux). A more extensive
sampling of shade shoots by Künstle and Mitscherlich (1975)
showed that, on average, Γi of P. menziesii was 0.66 times that
of P. sylvestris. Based on laboratory measurements (Leverenz
1995), I predicted that Γi of P. menziesii would be 0.53 times
that of P. sylvestris. Because the rates of dark respiration were
similar in the two species (Künstle and Mitscherlich 1976), the
differences in Γi are largely attributable to differences in shoot
structure (Leverenz 1995).
The apparent convexity (rate of bending, θa) for the
P. sylvestris (0.60) shoot was 0.61 times that of the P. menziesii
(0.98) shoot (Figure 1). A ratio of 0.23 is predicted from the
laboratory data of Leverenz (1995). The smaller difference in
θa in the field may reflect the more diffuse light environment
compared with that of the laboratory. However, low values of
θa (from 0.0 to 0.36) have also been reported for P. contorta
shoots (Rmax = 0.5) under natural illumination in the field (Dick
et al. 1991). The estimated light-saturated rate of photosynthesis (Asat , dry weight basis) was 35% higher in the P. sylvestris
shoot (10.7 mg g −1 h −1) than in the P. menziesii shoot (8.0 mg
g −1 h −1), which is in agreement with the laboratory results of
Leverenz (1995).
Hodges and Scott (1968) measured photosynthetic light
response curves of shoots of several conifer trees when illuminances were low and water stress minimal. Illuminance was
measured inside the chambers with selenium photocells. The
results of their measurements are reproduced in Figure 2. The
Figure 2. Net photosynthesis (An) in relation to illuminance for shoots
of six conifer species (redrawn from Figure 1 of Hodges and Scott
1968). The curve to the far left (1,2) is approximated from the overlapping curves for Tsuga heterophylla (Rmax = 0.85) and Abies grandis
(Rmax = 0.99). The other curves are for (3) Picea sitchensis (Rmax =
0.74), (4) Pseudotsuga menziesii (Rmax = 0.87), (5) Abies procera
(Rmax = 0.73), and (6) Pinus sylvestris (Rmax = 0.54). Rmax values are
the mean values reported by Leverenz and Hinckley (1990) and are
typically within ± 0.10 of the Rmax for individual shade shoots of a
given species.
light compensation point was about twofold higher, and the
initial slope was about twofold lower for P. sylvestris than for
Abies grandis Lindl. (Figure 2). Abies procera Rehd. had the
next highest Γi and next lowest φi followed by P. menziesii and
P. sitchensis. These rankings are in close agreement with the
laboratory results of Leverenz (1995) for unilaterally illuminated shoots. Within a species, the differences in φi values
between the field and laboratory measurements are attributable
to tree-to-tree variations in Rmax (Leverenz and Hinckley 1990,
Leverenz 1995).
Long-term photosynthetic production under the shade of a
forest stand has also been ranked with respect to species
(Table 1 in Hodges and Scott 1968) with A. grandis shoots
having the highest average rates during daylight hours, followed by Tsuga heterophylla (Raf.) Sarg., P. sitchensis,
P. menziesii, A. procera and lastly P. sylvestris. These results
support the contention that data from steady-state, unilateral
illumination in the laboratory can be used to infer relative
photosynthetic efficiency and performance under natural illumination when stress is minimized. The results on individual
shoots under natural illumination in the field are in agreement
with the hypotheses that shade-shoot structure itself strongly
affects photosynthetic production, the development of leaf
area, and production in dense conifer stands on fertile sites.
However, these results differ from the results reported by
Carter and Smith (1985) who found no strong effect of shoot
structure on photosynthesis at low irradiances, and the results
of Benecke (1980) and Dick et al. (1991) who reported high
quantum yields for pine shoots.
Maximum photosynthetic capacity
Among evergreen conifer species, there is a slight negative
correlation between Asat and Rmax for shade shoots (Leverenz
FIELD PHOTOSYNTHESIS AND SHADE-SHOOT STRUCTURE
1995), indicating that there is a negative correlation between
photosynthetic capacity and stand production. However, the
variations in Asat among species were small compared to the
variation within a species. A survey of the literature of the
maximum measured rates of photosynthesis (Amax ) of different
species with known Rmax also reveals that the ability to maintain high rates of photosynthesis under favorable conditions is
negatively correlated with the ability to produce shade shoots
with a high Rmax (Table 2). The correlation becomes even more
negative when the rates of photosynthesis are expressed per
unit of shoot projected area rather than leaf projected area,
because the species with the highest rates of photosynthesis
have the lowest Rmax .
Combining the data summarized by Leverenz (1992, Figure 2) and the data in Table 2 yields a significant negative
correlation between volume production (Gv,r , expressed as a %
of that of P. abies) and Amax (Gv,r = 156.2 − 5.41Amax , R2 = 0.77,
P = 0.009). These data support the hypothesis that, in dense
stands on fertile sites, efficiency of photosynthesis at low light
(which is strongly affected by shoot structure) is more important for stand production than maximum rate of photosynthesis
(which is strongly affected by biochemical differences per unit
leaf area), i.e., architectural variation is more important than
variation in leaf biochemistry in determining the variation in
growth and productivity among species (Küppers 1994, Leverenz 1995).
Acknowledgments
The Swedish Forest and Agricultural Research Council provided financial support.
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Table 2. Maximum measured photosynthetic rates (Pmax , µmol m −2
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© 1996 Heron Publishing----Victoria, Canada
Shade-shoot structure, photosynthetic performance in the field, and
photosynthetic capacity of evergreen conifers
JERRY W. LEVERENZ
Department of Ecology and Environmental Sciences, Swedish University of Agricultural Sciences, Box072,
7 S-750 07 Uppsala, Sweden
Current address: The Arboretum, The Royal Veterinary and Agricultural University, Kirkegaardsvej 3A,
DK2970 Hoersholm, Denmark
Received March 2, 1995
Summary Shoot structure can be quantified as the ratio of
maximum shoot silhouette area to maximum leaf silhouette
(projected) area (Rmax ). I have used published studies on the
effects of shade-shoot structure on photosynthetic production
of evergreen conifer stands to test the hypothesis that the lower
crown of stands of species with a high Rmax contributes significantly to photosynthetic production. Pruning studies were
found inadequate to test this hypothesis rigorously. Eight studies that used cuvettes to measure photosynthetic production in
different crown layers are reviewed. Of six studies on species
with Rmax values larger than 0.7, five found significant rates of
photosynthesis in the lower half of the crowns. In contrast,
pines, which have a low Rmax and a low leaf area index (≤ 3.5),
had low rates of photosynthesis in the lowest crown zone. In
field-grown shoots of all species examined, photosynthetic
capacity was negatively related to Rmax .
Keywords: field photosynthesis, leaf silhouette area, photosynthetic production, shoot silhouette area.
Introduction
Leverenz and Hinckley (1990) and Leverenz (1992) found
significant correlations between the architecture of shade
shoots (quantified as the ratio of maximum shoot silhouette
area to maximum leaf silhouette (projected) area, Rmax ) of
different evergreen conifer species and maximum leaf area
index, or maximum stand production. These correlations support the hypothesis that, in closed evergreen conifer stands, the
distribution and inclination of needles within shade-adapted
shoots has a major effect on maximum photosynthetic production and thus maximum stand production. However, this positive correlation does not hold on all sites, and species that are
more productive on good sites can be less productive on poor
sites (Aldhous and Low 1974). Thus shoot architecture can
affect the ability of a species to respond to variations in nutrient
availability or site water balance.
Leverenz and Hinckley (1990) hypothesized that species
that produce shade shoots with a high Rmax will be able to
develop a deeper canopy in terms of leaf area or leaf biomass
as a result of a lower light compensation point than shade
shoots with a low Rmax . It was also hypothesized that shade
shoots with a high Rmax will operate more efficiently at irradiances just above the light compensation point than shade
shoots with a low Rmax . This would result in significant photosynthetic production even at irradiances only slightly above
the light compensation point. I have reviewed the literature on
photosynthetic production at different canopy depths within
stand-grown trees to determine whether species that have a
high Rmax also have a high leaf area index and significant
photosynthetic production in their lower crowns. Conversely, I
have also examined whether species with a low Rmax have a low
leaf area index and negligible photosynthetic production in
their lower crowns.
Leverenz (1995) reported laboratory data indicating that
shade-shoot structure itself is responsible for the correlations
between Rmax and stand production through its effect on photosynthetic efficiency. In the same study, no clear effects of
variation in needle structure were observed. However, the
illumination used was strongly collimated or almost totally
diffuse, which is not the case in nature (Madgwick and Brumfield 1969, Grace 1971). Also, these laboratory measurements
were made under steady-state conditions, and it is not known
how natural fluctuations in irradiance with time may affect the
results. For example, under natural illumination, a pine shoot
may be no less photosynthetically efficient than a flat shoot
because the changing position of the sun results in shadows
that constantly move across individual cells of the needles, i.e.,
spatial and temporal variations in illumination direction may
compensate for differences in shoot structure so that, if the
pattern of shadows occurs with the right frequency, decreases
in photosynthesis as a result of mutual shading may be small
(Pearcy 1990). A second objective of this review, therefore,
was to survey the literature to test the hypothesis that photosynthetic performance in the field is related to shoot architecture.
Pruning experiments
Pruning or thinning experiments often result in the conclusion
that the lower crown of conifer canopies does not contribute
significantly to the production of the stand. For example,
Waring (1991) concluded that leaf area indices in excess of 6
are inconsequential for photosynthetic production. However,
110
LEVERENZ
based on a review of pruning experiments within forest stands,
Mar-Møller (1960) concluded the lower crown zones are important for photosynthetic production. He found that in cases
where pruning the lower branches from forest trees did not
decrease production, other factors were confounding the results. Thus in some studies, the foliage removed by pruning
was largely or completely replaced by regrowth, and so no
statistically significant effects of pruning were found. In other
studies, there was no measurable effect of pruning on stem
growth because pruning was done below the height on the stem
where diameter growth was measured (Margolis et al. 1988).
Mar-Møller (1960) also reported a study (Hartig 1872)
where severe drought in combination with pruning resulted in
an increase in production. It is probable that there is an optimal
leaf area index that is a function of site water balance (Gholz
et al. 1976, Linder 1985). Pruning of stands with a supra-optimal leaf area index as a result of drought stress should lead to
a less negative, or even a positive effect on growth. This would
occur when leaf water potentials drop below a critical water
potential for growth (Hsiao 1973) or photosynthesis (Aussenac
and Granier 1978, Beadle et al. 1981). Therefore, to interpret
accurately the results of pruning experiments, the effects of
limiting water on tree growth must be clearly separated from
the contribution of the lower canopy to photosynthetic production. There is good evidence that leaf area in evergreen conifers
is controlled by Rmax through its affect on the light compensation point (Leverenz and Hinckley 1990, Leverenz 1995).
Thus, it may be hypothesized that there is selection pressure
for a particular Rmax (low Rmax on drought-prone sites and high
Rmax on well-watered sites) to obtain an optimal leaf area for
maximizing tree growth and reproductive success.
Pruning of the lower crown zone may have little effect on
growth in some instances simply because only a small fraction
of the total leaf area or mass is removed. Oren et al. (1986)
found that, in Picea abies (L.) Karst., the lower 40% of the
canopy in terms of height contains only 5% of the foliage mass.
Similarly, in Pseudotsuga menziesii (Mirb.) Franco, the lower
25 to 30% of the canopy (based on whorl number) may contain
only 4 to 9% of the foliage mass (Jensen 1976, Brix 1981).
I conclude that most published pruning studies do not provide a critical test of the hypothesis that the lowest one-third
of the leaf mass or leaf area of a canopy contributes significantly to total canopy photosynthetic production.
Photosynthetic production within different crown zones
I found eight published studies on four species of evergreen
conifers that reported on variation in photosynthetic production with crown depth. The species studied were: P. menziesii
(Woodman 1971, Künstle and Mitscherlich 1975), P. abies
(Neuwirth 1968, Oren et al. 1986, Häsler 1992), Picea sitchensis (Bong.) Carr. (Watts et al. 1976), and Pinus sylvestris L.
(Neuwirth 1972, Künstle and Mitscherlich 1975, Beadle et al.
1985). Table 1 lists the results from this survey in order of
decreasing Rmax and decreasing maximum leaf area index.
Assuming the stands were not subject to severe stress, the LAI
was substantially more than 6 for all species except
Table 1. Relative photosynthetic production within different crown
zones of stand-grown trees.
Species
Percent of maximum photosynthesis
Dry weight basis
Area basis
Pseudotsuga menziesii (Woodman 1971)
Rmax = 0.87, LAImax = 13
Level 1 (top)
84%
Level 2
100%
Level 3
71%
Level 4 (bottom)
11%
Picea abies (Neuwirth 1968; combined results from extreme types
of comb and plate spruces)
Rmax = 0.84, LAImax = 11.5
Level 1 (top)
100%
Level 2
80%
Level 3
64%
Level 4 (bottom)
> 26%
Picea abies (Oren et al. 1986)
Rmax = 0.84, LAImax = 11.5
Level 1 (top)
Level 2
Level 3
Level 4 (bottom)
100%
97%
70%
52%
93%
100%
57%
33%
Picea sitchensis (Watts et al. 1976)
Rmax = 0.74, LAImax = 10.6
Level 1 (Nodes 1--3, top)
100%
Level 2 (Nodes 4--6)
99%
Level 3 (Nodes 7--8, bottom)
62%
100%
79%
42%
Pinus sylvestris (Neuwirth 1972)
Rmax = 0.54, LAImax = 3.5
Level 1 (12--15 m)
100%
Level 2 (9--12 m)
70%
Level 3 (6--9 m)
28%
Pinus sylvestris (Beadle et al. 1985)
Rmax = 0.54, LAImax = 3.5
Level 1(top)
Level 2 (middle)
Level 3 (bottom)
100%
66%
34%
P. sylvestris. The data of Häsler (1992) and Künstle and Mitscherlich (1975) are not listed in Table 1 because they sampled
at only two heights in the tree crowns and used a limited
number of cuvettes.
Based on the data reported by Woodman (1971) for
P. menziesii (Rmax = 0.87), photosynthetic production was only
negligible in the lowest crown zone (Level 4). This zone
contained 10% of the living branches of the tree, but less than
10% of the total foliage mass, and represented the zone where
shoots die for lack of light. The bulk of the crown (90%) had
rates of photosynthesis that were 70% of the zone with the
highest rates.
Similar results were obtained for P. abies (Rmax = 0.84)
based on the data in Figures 2 and 4 of the papers by Neuwirth
(1968) and Oren et al. (1986), respectively. In agreement with
Mar-Møller (1960), Neuwirth (1968) concluded that care
FIELD PHOTOSYNTHESIS AND SHADE-SHOOT STRUCTURE
should be taken not to underestimate the contribution of the
lower crown zone to the total photosynthetic production of the
entire crown. The study by Oren et al. (1986) showed that the
upper shade crown made a large contribution to photosynthetic
production per unit leaf area, especially when expressed per
unit of invested leaf mass (values obtained by dividing the
mean rates of photosynthesis by their mean specific leaf areas).
However, even in the lowest canopy zone, photosynthetic
production (dry weight basis) was 52% of that in the most
productive zone. Similarly, Häsler (1992) found that photosynthetic production (needle area basis) in the lower crown of a P.
abies tree was 56% of that in the upper crown. However, the
data reported by Häsler (1992) do not provide a rigorous test
of the hypothesis because it is unclear if the sampled trees were
growing in a closed stand.
A summary of data published by Watts et al. (1976) for
P. sitchensis is shown in Table 1. Rates of photosynthesis on an
area basis were calculated from their Figure 7, and data for the
same stand (Figure 7 in Norman and Jarvis 1974) were then
used to convert from an area to a mass basis. The relatively
high Rmax of 0.74 of P. sitchensis was associated with an LAI
substantially above 6 and with significant rates of photosynthesis (dry weight basis) in the lowest third of the crown (whorl
basis).
In contrast to the above five studies on species with shade
shoots with a high Rmax , Künstle and Mitscherlich (1975)
concluded that, in P. menziesii (Rmax = 0.87), the lower half of
the crown did not contribute significantly to photosynthetic
production. The reason for this discrepancy is unclear.
A comparison of the data for P. sitchensis, P. abies and
P. menziesii with the data for P. sylvestris (Rmax = 0.54) reported by Neuwirth (1972) and Beadle et al. (1985) indicated
that the lower crown zone of P. sylvestris was less productive
than the lower crowns of the other three species despite the
much lower LAI of the pine species. Both studies report that
photosynthetic production of the lowest crown zone was about
30% of that of the highest crown zone (Neuwirth 1972, Beadle
et al. 1985). Thus, the P. sylvestris canopies had both lower
LAI and lower rates of photosynthesis in their lower crown
compared with the upper crown. Unfortunately, it is not possible to relate these photosynthetic data for P. sylvestris to the
actual leaf area or leaf mass within the different canopy zones;
however, the maximum leaf area index for P. sylvestris is so
low (about 3, and at most 4) that the LAI of the total crown
would be equivalent to, or less than, the upper half of the
crowns of the other species. Nevertheless, there was still a
sharp decrease in photosynthetic performance with decreasing
crown depth in the P. sylvestris stands.
I conclude that five of these six studies support the hypothesis (Leverenz and Hinckley 1990) that species that produce
shade shoots with a high Rmax will have substantial rates of
photosynthesis in the bulk of their lower crowns despite having
an LAI of more than 6. Only the very lowest foliage (10% or
less of the total leaf mass) appears not to contribute significantly to total photosynthetic production.
111
Photosynthetic responses to light by individual shoots
To test the hypothesis that shoot architecture itself underlies
the observed differences in photosynthetic production. It is
necessary to test the effects under natural illumination. I compared the photosynthetic performance of different species
based on the following criteria: the initial slope of the irradiance response curve of photosynthesis (the maximum quantum
yield based on incident light), rate of dark respiration, light
compensation point, rate of bending of the light response curve
(apparent convexity), and maximum rate of photosynthesis
(Leverenz 1995).
Under nonstress conditions, the initial slope of the irradiance response curve of photosynthesis may be modeled as
(Leverenz 1995):
φi ≤ αφaRmax ,
(1)
where φi is the maximum initial slope (equivalent to apparent
quantum yield) based on incident irradiance, φa is the maximum initial slope based on absorbed irradiance or illuminance,
and α is leaf absorptance under the conditions of illumination.
Interceptance of irradiance will be reduced for all directions of
illumination other than the one that maximizes Rmax . This will
decrease the initial slope based on incident light. In the field,
φi will not be larger than φaRmax if the total irradiance at the
shoot is accurately estimated.
Troeng and Linder (1982) estimated that the mean maximum φi for P. sylvestris shoots in the field was 0.27 ± 0.002,
which when divided by 0.5 to correct for Rmax gives an estimated φa of 0.054. The expected quantum yield at 20 °C is
0.061 (Leverenz and Öquist 1987), which is about 12% higher
than predicted by Equation 1. On a projected needle area basis,
a φi of 0.052 is obtained from Figure 4 of the paper published
by Benecke (1980), which when divided by 0.5 to correct for
Rmax gives a φa of 0.104 compared with an expected yield at
17 °C of 0.063 (Leverenz and Öquist 1987). In this case, the
apparent quantum yield is 1.65 times higher than predicted by
Equation 1. Dick et al. (1991) also reported high φi values for
Pinus contorta Dougl. shoots.
One of the few comparisons of light response curves of
photosynthesis of different conifer species under natural illumination was made by Künstle and Mitscherlich (1970), who
compared the light response curves of shoots of P. menziesii
and P. sylvestris. The P. menziesii shoot probably did not
receive direct solar radiation until after 1500 h, whereas the
P. sylvestris shoot did not receive direct solar radiation in the
afternoon. Parameter values describing the curves were obtained by nonlinear least squares fitting of the convexity equation to these data (Figure 1). The estimated φi of the fitted curve
for P. sylvestris was 0.53 times the φi value for P. menziesii.
From a regression equation relating shoot architecture to φi
determined in the laboratory, Leverenz (1995) predicted a ratio
of 0.61 assuming Rmax values of 0.87 and 0.5 for the P. menziesii and P. sylvestris shoots, respectively. However, when the
field and laboratory φi values were corrected for possible
differences in specific leaf area between the two species:
112
LEVERENZ
Figure 1. Net photosynthesis (An ) in relation to illuminance for a
Pseudotsuga menziesii shoot (s) and a Pinus sylvestris shoot (d).
Illuminance was measured with a spherical sensor. Data points were
taken from Figure 5 in Künstle and Mitscherlich (1970). The solid
lines represent the best fit of the convexity equation to the data by
nonlinear least squares.
φi,weight ≤ αφaRmax /S,
(2)
where S is the specific leaf area in units of m2 g −1, the φi,weight
values determined from field measurements were not significantly different from those predicted from laboratory measurements.
The rates of dark respiration estimated by fitting the convexity equation were similar for the two species (0.12 mg g −1 h −1)
(cf. Hodges and Scott 1968, Leverenz 1995). The light compensation point (Γi) was twofold higher for P. sylvestris (1.2
Klux) than for P. menziesii (0.6 Klux). A more extensive
sampling of shade shoots by Künstle and Mitscherlich (1975)
showed that, on average, Γi of P. menziesii was 0.66 times that
of P. sylvestris. Based on laboratory measurements (Leverenz
1995), I predicted that Γi of P. menziesii would be 0.53 times
that of P. sylvestris. Because the rates of dark respiration were
similar in the two species (Künstle and Mitscherlich 1976), the
differences in Γi are largely attributable to differences in shoot
structure (Leverenz 1995).
The apparent convexity (rate of bending, θa) for the
P. sylvestris (0.60) shoot was 0.61 times that of the P. menziesii
(0.98) shoot (Figure 1). A ratio of 0.23 is predicted from the
laboratory data of Leverenz (1995). The smaller difference in
θa in the field may reflect the more diffuse light environment
compared with that of the laboratory. However, low values of
θa (from 0.0 to 0.36) have also been reported for P. contorta
shoots (Rmax = 0.5) under natural illumination in the field (Dick
et al. 1991). The estimated light-saturated rate of photosynthesis (Asat , dry weight basis) was 35% higher in the P. sylvestris
shoot (10.7 mg g −1 h −1) than in the P. menziesii shoot (8.0 mg
g −1 h −1), which is in agreement with the laboratory results of
Leverenz (1995).
Hodges and Scott (1968) measured photosynthetic light
response curves of shoots of several conifer trees when illuminances were low and water stress minimal. Illuminance was
measured inside the chambers with selenium photocells. The
results of their measurements are reproduced in Figure 2. The
Figure 2. Net photosynthesis (An) in relation to illuminance for shoots
of six conifer species (redrawn from Figure 1 of Hodges and Scott
1968). The curve to the far left (1,2) is approximated from the overlapping curves for Tsuga heterophylla (Rmax = 0.85) and Abies grandis
(Rmax = 0.99). The other curves are for (3) Picea sitchensis (Rmax =
0.74), (4) Pseudotsuga menziesii (Rmax = 0.87), (5) Abies procera
(Rmax = 0.73), and (6) Pinus sylvestris (Rmax = 0.54). Rmax values are
the mean values reported by Leverenz and Hinckley (1990) and are
typically within ± 0.10 of the Rmax for individual shade shoots of a
given species.
light compensation point was about twofold higher, and the
initial slope was about twofold lower for P. sylvestris than for
Abies grandis Lindl. (Figure 2). Abies procera Rehd. had the
next highest Γi and next lowest φi followed by P. menziesii and
P. sitchensis. These rankings are in close agreement with the
laboratory results of Leverenz (1995) for unilaterally illuminated shoots. Within a species, the differences in φi values
between the field and laboratory measurements are attributable
to tree-to-tree variations in Rmax (Leverenz and Hinckley 1990,
Leverenz 1995).
Long-term photosynthetic production under the shade of a
forest stand has also been ranked with respect to species
(Table 1 in Hodges and Scott 1968) with A. grandis shoots
having the highest average rates during daylight hours, followed by Tsuga heterophylla (Raf.) Sarg., P. sitchensis,
P. menziesii, A. procera and lastly P. sylvestris. These results
support the contention that data from steady-state, unilateral
illumination in the laboratory can be used to infer relative
photosynthetic efficiency and performance under natural illumination when stress is minimized. The results on individual
shoots under natural illumination in the field are in agreement
with the hypotheses that shade-shoot structure itself strongly
affects photosynthetic production, the development of leaf
area, and production in dense conifer stands on fertile sites.
However, these results differ from the results reported by
Carter and Smith (1985) who found no strong effect of shoot
structure on photosynthesis at low irradiances, and the results
of Benecke (1980) and Dick et al. (1991) who reported high
quantum yields for pine shoots.
Maximum photosynthetic capacity
Among evergreen conifer species, there is a slight negative
correlation between Asat and Rmax for shade shoots (Leverenz
FIELD PHOTOSYNTHESIS AND SHADE-SHOOT STRUCTURE
1995), indicating that there is a negative correlation between
photosynthetic capacity and stand production. However, the
variations in Asat among species were small compared to the
variation within a species. A survey of the literature of the
maximum measured rates of photosynthesis (Amax ) of different
species with known Rmax also reveals that the ability to maintain high rates of photosynthesis under favorable conditions is
negatively correlated with the ability to produce shade shoots
with a high Rmax (Table 2). The correlation becomes even more
negative when the rates of photosynthesis are expressed per
unit of shoot projected area rather than leaf projected area,
because the species with the highest rates of photosynthesis
have the lowest Rmax .
Combining the data summarized by Leverenz (1992, Figure 2) and the data in Table 2 yields a significant negative
correlation between volume production (Gv,r , expressed as a %
of that of P. abies) and Amax (Gv,r = 156.2 − 5.41Amax , R2 = 0.77,
P = 0.009). These data support the hypothesis that, in dense
stands on fertile sites, efficiency of photosynthesis at low light
(which is strongly affected by shoot structure) is more important for stand production than maximum rate of photosynthesis
(which is strongly affected by biochemical differences per unit
leaf area), i.e., architectural variation is more important than
variation in leaf biochemistry in determining the variation in
growth and productivity among species (Küppers 1994, Leverenz 1995).
Acknowledgments
The Swedish Forest and Agricultural Research Council provided financial support.
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113
Table 2. Maximum measured photosynthetic rates (Pmax , µmol m −2
s −1) of shoots of field-grown evergreen conifers. Rates are based on
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Species
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Source
Abies grandis
Pseudotsuga menziesii
Abies amabilis
Tsuga heterophylla
Picea abies
Picea sitchensis
Abies lasiocarpa
Pinus sylvestris
Pinus contorta
0.99
0.87
0.87
0.85
0.84
0.74
0.67
0.54
0.50
7.1
7.6
8.1
6.3
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11.4
8.5
17.4
15.6
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